Basic Appl. Ecol. 4, 79–85 (2003)
© Urban & Fischer Verlag
http://www.urbanfischer.de/journals/baecol
Basic and Applied Ecology
Costs of induced responses in plants
Don Cipollini1,*, Colin B. Purrington2 and Joy Bergelson3
1
Department of Biological Sciences, Wright State University, Dayton, Ohio, USA
Department of Biology, Swarthmore College, Swarthmore, Pennsylvania USA
3
Department of Ecology and Evolution, University of Chicago, Chicago, Illinois USA
2
Received November 1, 2001 · Accepted February 15, 2002
Abstract
Induced responses to herbivores in plants are thought to be a form of adaptive phenotypic plasticity,
whereby plants save metabolic costs by expressing defenses only when they are necessary. Although
costs of being inducible have never been examined, there have been many studies of costs of induced
responses, with approaches ranging from the manipulation of induction with herbivores or wounding, and more recently, with chemical elicitors. While some early studies reported no significant
costs of induced responses, evidence for significant costs of induced responses in both wild and agricultural species has recently increased in the literature. Recent studies have made it clear that benefits of induced responses in the field in the presence of herbivores can counterbalance costs of induced responses seen in the absence of herbivores. Moreover, as has been shown for constitutive resistance, costs of induced responses may vary with environmental conditions, including the presence
of competitors and altered resource availability. Ecological costs of induced responses may include
increased susceptibility to untargeted herbivores, either through the altered attraction of specific
herbivores or due to defense pathway cross-talk, but the actual fitness consequences of such ecological costs have been little studied. Mutant and transgenic plants altered in induced responses are increasingly being identified or produced, as are specific elicitors of direct and indirect defenses. Their
use, coupled with the increasing ability to analyze global gene expression in plants, will advance
studies on the specificity, magnitude, and mechanisms of costs of induced responses.
Induzierte Antworten von Pflanzen auf Angriffe durch Herbivore werden als eine Form adaptiver
phänotypischer Plastizität betrachtet, wobei Pflanzen metabolische Kosten sparen, wenn sie Abwehr nur dann mobilisieren, wenn sie auch wirklich benötigt wird. Während Kosten der Induzierbarkeit bisher nie untersucht wurden, gibt es viele Studien zu Kosten von induzierten Antworten. In
diesen Studien wird Induktion durch Herbivore, mechanische Verwundung, oder durch chemische
Elicitoren manipuliert. Während einige erste Studien keine signifikanten Kosten der induzierten
pflanzlichen Antworten fanden, ergaben neuere Untersuchungen Anhaltspunkte für deutliche
Kosten der Induktion sowohl bei Wild- wie auch bei Kulturpflanzen. Die neueren Studien zeigen
deutlich, dass der Nutzen, der aus induzierten Antworten in Gegenwart von Herbivoren gezogen
werden kann, die Kosten ausbalanciert, die in Abwesenheit von Herbivoren investiert werden.
Ebenso wie konstitutive Resistenz kann auch die induzierte Antwort mit den verschiedenen
Umweltfaktoren wie z.B. Konkurrenz und Nahrungsverfügbarkeit variieren. Die ökologischen
Kosten induzierter Antworten können auch zu einer erhöhten Anfälligkeit gegenüber solchen
spezialisierten Herbivoren führen, die durch die induzierte Antwort sogar angelockt werden. Weitere, allerdings bisher wenig untersuchte ökologische Kosten könnten dadurch entstehen, dass
Wechselwirkungen zwischen induzierten Abwehr-Biogenesewegen auftreten. Pflanzenmutanten
*Corresponding author: Don Cipollini, Department of Biological Sciences, Wright State University, Dayton, Ohio, 45435 USA,
Phone: +1-937-775-3805, Fax: +1-937-775-3320, e-mail: don.cipollini@wright.edu
1439-1791/03/04/01-079 $ 15.00/0
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Cipollini et al.
oder transgene Pflanzen mit veränderter induzierter Antwort werden mehr und mehr identifiziert
oder produziert. Auch der Kenntnisstand über Elicitoren der direkten und indirekten Verteidigung
erweitert sich zunehmend. Wenn genetisch veränderte Pflanzen genutzt werden und die Kenntnisse
über die Elicitoren ebenso eingesetzt werden wie die Fähigkeit zur Analyse der Genexpression in
Pflanzen, dann können die Untersuchungen zur Spezifität, zum Ausmaß, und den Mechanismen
der Kosten von induzierten Antworten der Pflanzen auf Herbivorenbefall Fortschritte machen.
Key words: costs of resistance – elicitors – herbivores – pathogens – systemic acquired resistance –
transgenic plants
Introduction
It is widely assumed that the constitutive expression of
resistance in plants is accompanied by fitness costs
that accrue when pests and pathogens are absent
(Rhoades 1979, Simms & Rausher 1987, Herms &
Mattson 1992, Simms 1992, Bergelson & Purrington
1996, Purrington 2000). The magnitude of these costs
may explain why susceptible genotypes persist in
many plant populations (Dirzo & Harper 1982,
Berenbaum et al. 1986, Jones 2001). Inducible resistance, whereby plants mount morphological or biochemical defenses only when they are attacked, is a
form of adaptive phenotypic plasticity that may allow
plants to minimize fitness costs of resistance (Karban
& Baldwin 1997, Baldwin 1998, 1999, Cipollini
1998, Agrawal 1999, Agrawal et al. 1999b). The role
of costs in the evolution of induced responses is examined in more detail by Zangerl (2003). Because
agronomists and others frequently consider the ability
to induce a resistance response “cost free”, it is important to emphasize that there are well-documented
costs associated with induced responses. Recent reviews on costs of resistance in plants have given increased attention to costs of induced responses
(Purrington 2000, Heil 2001, Heil & Baldwin 2002).
The aim of this review is to highlight the current state
of knowledge on costs of induced responses in plants
and to explore directions in which future experimental
investigations are likely to focus. While recent research
has shown that plants can exhibit induced responses
to ovipositing herbivores (Meiners & Hilker 2000,
Hilker et al. 2002), the emphasis of this review is on
costs of plant responses to feeding herbivores, with
some discussion of responses induced by pathogens.
The cost of an induced response is typically measured as a reduction in plant fitness (e.g., survivorship
and seed production) in the absence of herbivores that
is due to the production of elevated levels of defense.
These costs are generally envisioned to be due to allocation of resources toward defense production and
away from primary metabolism (Bazzaz et al. 1987,
Herms & Mattson 1992). Another source of costs, in-
Basic Appl. Ecol. 4, 1 (2003)
voked sometimes in the context of constitutive resistance, is autotoxicity of defensive chemicals (McKey
1974, Baldwin & Callahan 1993). Negative effects of
induced responses on a plant’s interaction with other
plants, plant consumers, or plant mutualists are referred to as “ecological” costs, and have been the
focus of several recent studies and reviews (Felton et
al. 1999, Thaler et al. 1999, Felton & Korth 2000,
Heil 2001, Cipollini 2002a, Siemens et al. 2002).
Costs of simply being inducible, which would be reflected in costs of inducibility in the absence of induction and in the absence of herbivore attack, have never
been examined (Bergelson & Purrington 1996,
Cipollini 1998, Purrington 2000).
Wounding has often been used to assess
costs of induced responses
Typically, studies on costs of induced responses have
involved the controlled application of an insect herbivore to induce a response, followed by its removal and
an assessment of the performance of the plant. This approach is sometimes accompanied by measurement of
putative morphological or biochemical defenses, or by
an assessment of levels of resistance achieved by the induction in a bioassay. In some cases, the occurrence of
natural damage early in the season is simply correlated
with both later damage (to estimate the induction of resistance by early damage) and plant fitness (Karban
1993). While biologically realistic, this latter approach
can be ripe with flaws. First, the distribution of damage early in the season can be affected by initial variation in constitutive or inducible defenses, which can in
turn be affected by differences in plant age, genotype or
growing conditions (Alarcon & Malone 1995, Bolter
et al. 1998, Siemens & Mitchell-Olds 1998, Cipollini
& Redman 1999, Cipollini & Bergelson 2000, 2001,
Cipollini 2002b). These confounding effects can lead
to unknown biases. Second, even if plants receive a
similar amount and pattern of damage, there can be a
great degree of specificity in induced responses to different herbivores, even in controlled laboratory experi-
Costs of induced responses in plants
ments on closely related individuals (Stout et al. 1998,
Stout & Bostock 1999, Agrawal 2000, Dicke et al.
2003). Any study that pools all herbivore damage, especially damage inflicted by different feeding styles,
would miss potentially important sources of variation.
This variability makes it important that defensive traits
are assessed directly in cost studies to insure that plants
are indeed induced. It also suggests that the presence
and magnitude of costs are highly dependent upon the
identity of the inducing organism, even in controlled
laboratory experiments.
Mechanical wounding itself has been shown to induce resistance in many plants and has been used in
several studies on costs. Indeed, a fitness cost associated with the induction of nicotine in tobacco by mechanical wounding was one of the first demonstrations
of fitness costs of an induced response (Baldwin et al.
1990). Using this approach, it is possible to carefully
control the amount, timing, and pattern of inducing
damage. The disadvantage is that mechanical wounding often does not cause the same induced responses as
actual herbivory (Baldwin 1990, Stout et al. 1998,
Stout & Bostock 1999, Dicke et al. 2003). In studies
utilizing some form of damage, either natural or artificial, to induce a response, it can also be difficult to account for costs produced by the damage itself (i.e. fitness decreases due to removal of resources stored in
plant tissues and by loss of assimilatory tissues). Fitness costs of damage are known to vary with plant
genotype, plant and leaf age, and environment (e.g.,
Rosenthal & Kotanen 1994). In some plants, rapid
whole-leaf removal (as opposed to persistent mechanical damage or herbivore feeding) does not induce resistance traits (Agrawal et al. 1999b, Cipollini & Sipe
2001), allowing some authors to use leaf damage
treatments to control for costs of leaf removal itself
(Agrawal et al. 1999b). In the absence of such controls, other authors have used techniques, such as pin
pricks, that effectively induce the plant with a minimum of leaf area loss and physical damage (Zangerl
et al. 1997).
Chemical elicitors of induced responses
are increasingly being used
Chemical elicitors capable of stimulating induced responses have been used in numerous studies. Brown
(1988) used chitin injections to induce defense responses in tomato in one of the first studies to assess
fitness costs of an induced response. Since this study,
the identification of signaling molecules, such as jasmonic acid (JA), that regulate the wound-inducible expression of defense genes (Creelman et al. 1992,
Farmer et al. 1992, McConn et al. 1997), has ad-
81
vanced the study of costs of induced responses. In fact,
the application of JA or its methyl ester to induce defenses has now been employed in numerous recent cost
studies (e.g., Baldwin 1998, van Dam & Baldwin
1998, 2001, Agrawal et al. 1999b, Thaler 1999,
Cipollini & Sipe 2001, Redman et al. 2001, Cipollini
2002a). Costs of induced responses to the application
of molecules that regulate other inducible resistance
pathways, such as salicylic acid (SA) or its mimics, are
also increasing in the literature (Tally et al. 1999, Heil
et al. 2000, Cipollini 2002a). The relative delay in
studies on costs of SA-induced responses is surprising,
however, given the multitude of studies on the role of
SA in systemic acquired resistance to pathogens (e.g.
Delaney et al. 1994, Delaney 1997, Mauch-Mani &
Metraux 1998, Heil 1999, 2001).
The manipulation of chemical elicitors offers the
advantage of uncoupling costs of induced responses
from the less controllable (and typically unmeasured)
costs of damage, and enables a high degree of control
over the spatial and temporal aspects of induction.
Moreover, application of different doses of an elicitor
allows for the quantitative assessment of costs (Baldwin 1998, Redman et al. 2001, Cipollini 2002a).
Gauging the correct amount of elicitor to apply to reasonably mimic that produced endogenously in response to damage can be a challenge, however, and requires knowledge of elicitor uptake and metabolism in
planta. Some authors have done a good job of this
(Baldwin et al. 1997), although most have just used estimates based on the degree to which certain levels of
elicitor induce resistance. Regardless, extending defense phenotypes beyond the average with high doses
of elicitor can still provide valuable information about
costs, and might provide forecasts about the effects of
engineering constitutive expression of inducible resistance in transgenic plants.
Despite its advantages, the use of chemical elicitors
possesses flaws of its own. First, signal transduction
cascades that are part of the induction of defense (e.g.
mitogen-activated protein kinase cascades) are mediated by numerous molecules, many of which interact in
complex ways (Xu et al. 1994, Thomma et al. 1998,
Tena et al. 2001). Application of one mediator of these
signaling cascades that, for example, exerts its effects
only midway through a pathway may not fully, or not
properly, initiate a biologically relevant resistance phenotype. Second, chemical elicitor treatment may produce secondary effects on plant primary or secondary
metabolism that can in turn affect plant fitness. For
example, in addition to its effects on defense expression, JA is known to affect processes ranging from
photosynthesis to pollen fertility (Creelman & Mullet
1997). However, because increased levels of endogenous JA are required for many defense responses
Basic Appl. Ecol. 4, 1 (2003)
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Cipollini et al.
(Baldwin et al. 1997, Creelman & Mullet 1997), it is
important to remember that secondary effects would
presumably make up some portion of the true cost of
naturally-induced responses.
Identification of specific elicitors of induced responses found in insect oral secretions, such as volicitin from
Spodoptera exigua (Alborn et al. 1997, Turlings et al.
2000), and the fatty acid – amino acid conjugates identified in Manduca sexta (Halitschke et al. 2001), offer
the opportunity to more closely mimic events associated with herbivore attack (Baldwin & Preston 1999, Felton & Korth 2000, Kahl et al. 2000, Halitschke et al.
2001, Voelckel et al. 2001a). The addition of these elicitors to mechanical wounds is often necessary and sufficient to mimic herbivore-induced responses (e.g. Halitschke et al. 2001), explaining why responses to mechanical damage alone are often different than those induced by herbivore damage. Because such elicitors
would influence a pathway from the detection of damage onward, they may reveal additional costs that are
underestimated using other elicitors. Use of specific
elicitors might also be expected to allow more precise
estimation of costs associated with resistance to a particular species, rather than the costs of induction associated with either mechanical damage or elicitors that invoke general or multiple resistance. Their use may also
reveal additional control points where inducible response pathways are regulated by the plant or by the
herbivore (Kahl et al. 2000, Voelckel et al. 2001a). Numerous elicitor molecules from plant pathogens have
been identified (e.g. harpin from Erwinia amylovora,
Wei et al. 1992) and have been used to probe hostpathogen interactions (Heath 2000, Tuzun 2001).
These elicitors would presumably have the same utility
in cost studies as molecules such as volicitin, but they
have not yet been applied in this context.
Plants used to study costs have varied
with the approach
As approaches to manipulating induced responses
have varied, so have the study subjects. The most complete studies of costs of induced responses have been
done on wild herbaceous plants, such as wild parsnip
(e.g. Zangerl et al. 1997), wild tobacco (e.g. Baldwin
1998) and wild radish (e.g. Agrawal et al. 1999b).
However, numerous studies have also been done on
agricultural crops, such as tomato (e.g. Brown 1988,
Thaler 1999, Thaler et al. 1999, Redman et al. 2001),
cultivated tobacco (e.g. Baldwin et al. 1990), and
wheat (e.g. Heil et al. 2000). Studies on agricultural
crops could be biased by artificial selection regimes for
yield and resistance traits, but the results of these studies have generally supported those found in wild
Basic Appl. Ecol. 4, 1 (2003)
plants. Arabidopsis thaliana has been used in several
studies of costs of constitutive resistance (Purrington
& Bergelson 1997, Mauricio 1998), but it was used
for the first time to study costs of induced responses
only recently (Cipollini 2002a). Although there is considerable interest in the inducible resistance phenotypes of trees (e.g., Haukioja & Honkanen 1997,
Clérivet & Alami 1999), no study of costs of induced
responses for a woody plant has yet been reported,
likely because of the difficulty in estimating fitness in
long-lived plants. Defense costs and benefits are believed to explain patterns of constitutive resistance in
long-lived woody plants across species and resource
environments (Feeny 1976, Coley et al. 1985). The
fact that damage-induced increases in thorn length in
Acacia drepanolobium will eventually relax after the
removal of herbivores suggests that costs may modulate the expression and distribution of induced responses in woody plants as well (Young & Okello
1998). Obviously, the assessment of costs of induced
responses needs to occur over much longer temporal
scales in woody plants than in short-lived herbaceous
plants.
As work on the molecular genetics of inducible response pathways has progressed, numerous mutants
that vary in their competence to induce resistance have
either been identified or produced using transgenic
technology (e.g. Delaney 1997, Cao et al. 1998). Manipulation of such experimental subjects provides a
novel way to assess costs (and benefits) of inducible responses in plants (Voelckel et al. 2001b, Cipollini
2002a). For example, manipulation of non-inducible
mutants (e.g. Staswick et al. 1992, Delaney et al.
1995) with an elicitor enables the assessment of secondary effects of elicitors on plant fitness that are unrelated to defense expression (Purrington 2000,
Cipollini 2002a). In turn, assessment of the fitness of
mutants that constitutively express inducible responses (e.g. Cao et al. 1998, Cipollini 2002a) would provide information on costs of high levels of defense expression and autotoxicity. The costs of induction,
while being interesting to evolutionary biologists, are
of applied importance to crop breeders attempting to
produce high-yielding yet well-protected crops. One
rather easy way to produce plants with induced resistance is to spray crop fields with chemical elicitors,
many of which are available commercially (e.g., Actigard®/BION® from Novartis) and that can invoke
costs such as those detailed above (Tally et al. 1999,
Heil et al. 2000, Oostendorp et al. 2001). A second
strategy is to clone genes involved in pest perception,
or subsequent signalling cascades, and engineer them
with strong promoters prior to plant transformation, a
strategy that would also entail costs of constitutively
expressing resistance genes (but see Cao et al. 1998).
Costs of induced responses in plants
Costs have been estimated in numerous ways
An ongoing debate on costs of resistance has centered
on the currency of cost. Because interest in costs of resistance is generally motivated by a desire to understand evolutionary dynamics, most studies have quantified costs using correlate(s) of fitness such as plant
size, flower production, pollen production, fruit and
seed production, fruit ripening, and seed germination
(e.g. Baldwin 1998, Agrawal et al. 1999b, Redman et
al. 2001, Cipollini 2002a). However, by examining
only fitness correlates, the mechanisms leading to
changes in fitness can not be determined at a physiological level (Gershenzon 1994, Purrington & Bergelson 1999). Other traits examined in studies on costs of
induced responses have included physiological traits
such as photosynthesis, respiration, and nitrogen uptake and utilization (Zangerl et al. 1997, Baldwin et
al. 1998, Baldwin & Hamilton 2000, van Dam &
Baldwin 2001). In studies that address costs of induced responses in a purely agricultural context, the
relevant trait to measure may be some aspect of vegetative growth or plant “quality”, rather than a more
direct measure of fitness (Thaler 1999, Tally et al.
1999).
With so many potential traits to measure, it is obvious that the choice of the measured trait and the focus
on certain defenses can determine the outcome of the
study. For example, Agrawal et al. (1999b) found that
responses induced by JA in wild radish had no effect on
female fitness traits, but negatively affected male fitness traits such as pollen production. Because female
fitness has been assessed much more frequently than
male fitness in studies of costs of induced responses,
many effects on male fitness have likely been missed.
Moreover, Agrawal (2001) found that responses induced by herbivores in wild radish can extend into the
next generation, suggesting that some costs of induced
responses in maternal plants may not show up until the
performance of their offspring can be assessed. The
magnitude of costs to any given fitness trait can potentially be influenced by many factors, including the degree of induction, mechanism of resistance, and environmental conditions. For example, the effects of reduced nutrient availability on costs of induced responses may be more pronounced on female fitness than on
male fitness. This makes it difficult to broadly compare
the magnitude of costs of induced responses between
different plants, environments, and responses. When
defense levels have been quantified and associated with
costs, the emphasis in empirical studies has been on the
expression of direct defenses. On the other hand, it has
been suggested that employment of indirect defenses,
such as the induced release of predator- or parasitoid-
83
attracting volatiles (Dicke et al. 1990, Alborn et al.
1997, DeMoraes et al. 1998, Turlings et al. 2000,
Dicke et al. 2003), may be metabolically cheaper than
the employment of direct defenses (Dicke & Sabelis
1992). The two attempts to estimate the metabolic
costs of induced volatiles have indeed substantiated
this claim (Dicke & Sabelis 1989, Halitischke et al.
2000). No study has yet empirically addressed these
costs in terms of fitness, however, although protocols
to assess their costs would likely be similar to those
used to assess costs of direct defenses. Induced indirect
defenses have been less well-studied than induced direct defenses, but plants are not restricted to producing
only one or the other. In fact, direct and indirect defenses may act synergistically to protect the plant
(Baldwin & Preston 1999). If plants produce both direct and indirect defenses in response to damage, then
some portion of fitness costs of induced responses may
be due to the production of predator-attracting
volatiles that have gone unmeasured in most studies. In
fact, it is possible to experimentally manipulate and assess costs of direct and indirect defenses in some systems where mechanical damage and herbivore damage
differentially induce direct and indirect defenses (Dicke
et al. 1990, Kahl et al. 2000). The most important
costs of the employment of induced predator-attracting
volatiles, however, may be due to the risk that herbivores would use such cues in long-range host detection
or host avoidance (Takabayashi & Dicke 1996, Dicke
& Vet 1999, Baldwin & Preston 1999, DeMoraes et al.
2001, Kessler & Baldwin 2001). In turn, because the
benefits to the plant of the production of induced
volatiles are highly dependent upon the predator and
parasitoid community, reliance on indirect defenses
may be costly if no protectors are there to respond to
alarm signals. Two recent studies have indicated that
under the right circumstances, however, parasitoid attraction can benefit fitness of induced plants (van Loon
et al. 2000, Hoballah-Fritzche & Turlings 2001).
Costs are increasingly being reported
although mechanisms are often unknown
While some early studies reported no significant costs
of induced responses (Brown 1988, Karban 1993), evidence for significant fitness costs of induced responses
has increased in the literature in the last four years
(e.g. Heil & Baldwin 2002). This may represent better
experimental control (perhaps through the use of specific elicitors on single genotypes of plants), use of elicitors with more secondary effects on metabolism and
growth, or a bias against the publication of studies
where insignificant costs have been found. Regardless
of the system, most studies on costs have been unable
Basic Appl. Ecol. 4, 1 (2003)
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Cipollini et al.
to determine the exact mechanism responsible for reduced fitness in plants expressing inducible defenses,
although resource allocation tradeoffs have been most
widely supported. For example, Zangerl et al. (1997)
were able to directly associate damage-induced increases in respiration rate and reductions in growth in
wild parsnip with the energetic costs of induced furanocoumarin production. In tobacco, damage-induced
increases in nicotine content can account for 6% of
the plant’s total nitrogen (Baldwin et al. 1998), and
high levels of nicotine can be autotoxic (Baldwin &
Callahan 1993). Because induction typically leads
plants to alter the production of numerous proteins,
compounds, and structures, it is not surprising that it
is difficult to quantitatively associate costs with the expression of particular defenses. Recent experiments
utilizing either differential display or microarrays to
analyze gene expression have shown that induction by
wounding or insect feeding in plants usually involves
the coordinate upregulation of many defense-related
transcripts, and the downregulation of transcripts involved in primary metabolism or other “housekeeping” roles (Reymond et al. 2000, Hermsmeier et al.
2001). This finding supports the long-held assumption
that, upon induction, resources are allocated toward
defense and wound healing, and away from primary
metabolism; redirections that can lead to fitness costs.
Understanding patterns of expression of genes after induction provides targets for genetic manipulation,
whereby individual genes can be up- or down-regulated to see which are most important in resistance, and
which are most costly (Delaney 1997, Martin 1999,
Melchers & Stuiver 2000, Kuc 2001, Tuzun 2001,
Voelckel et al. 2001b).
In order to consider inducible responses adaptive, it
is necessary that a benefit of induced responses in the
field can be demonstrated. Fitness benefits of induced
resistance have only rarely been measured, but at least
a couple of recent studies make clear that such benefits
in the presence of herbivores can counterbalance costs
of induced responses seen in the absence of herbivores
(Agrawal 1998, 1999, Baldwin 1998). The inability to
control (potentially unknown) benefits of induced responses could have contributed to the lack of significant costs of induced responses reported in some studies (Brown 1988, Karban 1993).
Costs may be contingent upon
the environment
Ecological costs of induced responses may include increased susceptibility to untargeted herbivores, either
through the altered attraction of specific herbivores or
due to defense pathway cross-talk that may alter re-
Basic Appl. Ecol. 4, 1 (2003)
sponsiveness to certain attackers. For example, cucumber plants induced to produce cucurbitacins may
become more resistant to generalist arthropod herbivores, but more susceptible to specialist beetles that
use cucurbitacins as feeding stimulants (Agrawal et al.
1999a). The same could be said for glucosinolates,
which tend to deter generalist arthropod herbivores
but may be used as oviposition stimulants and host acceptancenes by specialist lepidopterans (Renwick &
Lopez 1999, Siemens et al. 2002). The sometimes-negative interaction between SA- and JA-mediated inducible response pathways could make plants more resistant to some herbivores but more susceptible to others (Doares et al. 1995, Felton et al. 1999, Thaler et al.
1999, Felton & Korth 2000). The fitness consequences
of such ecological costs of induced responses have not
yet been demonstrated. However, evolutionary maintenance of the apparent prioritization of SA-mediated
responses over JA-mediated responses when both are
induced suggests that activation of these pathways
may vary in costliness or in effectiveness.
As has been shown for constitutive resistance (e.g.
Bergelson 1994), costs of induced responses may vary
with growing conditions, including the presence of
competitors and otherwise altered resource availability. For example, Heil et al. (2000) showed that induction of pathogen defense in wheat with BION®, an
elicitor that mimics the action of SA, was most costly
under nitrogen deprivation. An interesting set of recent studies with tobacco have indicated that the
neighbors of focal plants induced with JA benefit because they take advantage of temporary reductions in
the ability of induced plants to compete for nitrogen
(van Dam & Baldwin 1998, 2001, Baldwin & Hamilton 2000). This makes induction not only costly to the
induced focal plant but also beneficial to the neighbors. In contrast, other studies have found little effect
of external resource levels on costs of induced responses. Brown (1988) found that nitrogen availability (manipulated according to several regimes) had no effect
on costs of induced responses in tomato. Recent studies on Arabidopsis, Arabis, and Brassica have found
that defense responses induced by chemical elicitors or
insect herbivory were either no more costly or were
less costly in competing plants than in plants grown
alone (Cipollini 2002a, Siemens et al. 2002, D. Siemens,
unpublished data). These authors suggested that
pleiotropic effects of the signal molecules may have
had positive effects on competitive ability in induced
plants, or that some of the “anti-herbivore” defenses
induced in these plants served a direct role in competition. For example, elevated glucosinolate level is a
common inducible response in the Brassicaceae, of
which each of these plants are members. Glucosinolates can possess allelopathic properties (Brown &
Costs of induced responses in plants
Morra 1995, Siemens et al. 2002), and may benefit an
induced plant by suppressing the growth of neighboring vegetation if they are released from the roots. Such
benefits could either wholly or partially obscure the
known costs of their production (e.g. Mauricio 1998,
Stowe 1998, Siemens et al. 2002) when expressed in
certain ecological contexts. Such benefits are likely to
be species-specific and dependent upon the mechanism
of resistance, however, as is suggested by the fact that
uninduced tobacco plants benefit from induction of
their neighbors (van Dam & Baldwin 1998, 2001,
Baldwin & Hamilton 2000). In any case, it is clear
that the long-held assumption that competition or resource deprivation will increase fitness costs of resistance (Bazzaz et al. 1987) is not always supportable.
Costs of inducibility remain unexamined
Despite the general interest in examining the costs of
induction, there are a variety of costs of inducibility
that are often ignored, yet are potentially large (Bergelson & Purrington 1996, Cipollini 1998, Purrington
2000). These mechanisms include the production and
maintenance of sensing, response, and defense storage
systems, the production of enzymes that can protect
from autotoxicity, and lag-time costs (DeWitt et al.
1997, Glazebrook 2001, Tena et al. 2001). These
mechanisms could make phenotypic plasticity in resistance no less costly than the expression of constitutive
resistance, but perhaps more effective in other ways
(e.g., there might be a benefit in avoiding the simultaneous production of compounds that separately are effective against particular pests) (Karban et al. 1997,
see Zangerl 2003). In some amphibians (e.g. wood
frogs), costs of plasticity in the induction of a predator-induced phenotype can be widespread (Relyea
2002). To date, no published study on plants examines
whether there are detectable genetic or phenotypic
costs of phenotypic plasticity in herbivore resistance. It
would likely be difficult to separate such costs from
costs associated with the actual expression of constitutive or inducible defenses without careful control over
induction, and would require comparison of closely
related genotypes (or genetically manipulated genotypes) that vary only in defense plasticity. Because it is
believed that many inducible response pathway mechanisms may have been co-opted from other plant developmental processes (Tena et al. 2001), the component of costs due to the production and maintenance
of some signaling systems may be minimal (Cipollini
1998). Phenotypic plasticity in inducible defenses may
minimize fitness costs of resistance by limiting the expression of defense, but it may be accompanied by
unique costs in itself.
85
Polymorphism in induced resistance has been identified quite frequently in agricultural crops. In fact, the
rate and level at which crop genotypes can mount inducible defenses, or the identity of the defenses produced, often differentiates “susceptible” vs. “resistant”
cultivars (e.g., Hammerschmidt et al. 1984, Velozo
et al. 1999, Forslund et al. 2000). Polymorphism in induced responses has been examined less frequently in
wild plants, although it has been detected in a few
studies (Zangerl & Berenbaum 1990, van Dam &
Vrieling 1994, Bergelson et al. 2001, Glazebrook
2001). Polymorphisms in induced resistance to particular attackers may arise through variation in the
recognition of herbivore and pathogen presence, variation in signal transduction networks and metabolic
pathways controlling synthesis of defenses, and variation in effective deployment of defense. If induced responses themselves can vary among plant genotypes
within species, then genotypes may also vary in costs
of induced responses. This would be especially true if
cost-saving mechanisms exist and genotypes employ
them differentially. Agricultural plant genotypes that
can exhibit high levels of induced resistance at minimal costs to yield would be highly desirable to identify.
Unfortunately, such polymorphism has never been examined in either agricultural or wild plants.
Conclusions
The ability to experimentally manipulate the expression
of induced responses in plants has led to several recent
demonstrations of costs of resistance in plants, although the mechanisms of costs remain elusive. Induced indirect defenses have received much attention
recently, but their fitness costs have gone unmeasured,
as have the fitness consequences of ecological costs of
induced responses. Continued identification of specific
elicitors of induced responses, incorporation of response mutant and transgenic plants, and the analysis
of global gene expression in plants will increase the
ability of researchers to determine the mechanisms and
magnitude of costs of induced responses. The best studies will examine costs in ecologically-relevant contexts
to examine the contingencies of costs and benefits of induced responses, and the fitness effects of ecological
costs. Studies that examine costs of induced responses
over multiple spatial and temporal scales, and in woody
plants are needed, as are studies on costs of inducibility.
Progress in the study of costs of induced responses is
not only interesting to evolutionary ecologists, but also
important to agronomists interested in maximizing resistance and yield in cultivated plants where the phenotypic and genetic manipulation of induced responses as
a resistance strategy has become increasingly popular.
Basic Appl. Ecol. 4, 1 (2003)
86
Cipollini et al.
Acknowledgements. We thank Monika Hilker, Marcel
Dicke, Martin Heil and one anonymous reviewer for helpful
comments on the manuscript. We acknowledge financial
support during the writing of this manuscript from USDA
NRI-CGP grant 01-02783 (to D.C.), and NIH grants
GM57994 and GM62504 (to J.B.).
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